Genome Content and Phylogenomics Reveal both Ancestral and Lateral Evolutionary Pathways in Plant-Pathogenic Streptomyces Species

Abstract

e Streptomyces spp. are highly differentiated actinomycetes with large, linear chromosomes that encode an arsenal of biologically active molecules and catabolic enzymes. Members of this genus are well equipped for life in nutrient-limited environments and are common soil saprophytes. Out of the hundreds of species in the genus Streptomyces, a small group has evolved the ability to infect plants. The recent availability of Streptomyces genome sequences, including four genomes of pathogenic species, provided an opportunity to characterize the gene content specific to these pathogens and to study phylogenetic relationships among them. Genome sequencing, comparative genomics, and phylogenetic analysis enabled us to discriminate pathogenic from saprophytic Streptomyces strains; moreover, we calculated that the pathogen-specific genome contains 4,662 orthologs. Phylogenetic reconstruction suggested that Streptomyces scabies and S. ipomoeae share an ancestor but that their biosynthetic clusters encoding the required virulence factor thaxtomin have diverged. In contrast, S. turgidiscabies and S. acidiscabies, two relatively unrelated pathogens, possess highly similar thaxtomin biosynthesis clusters, which suggests that the acquisition of these genes was through lateral gene transfer.

TxtH is a key component of the thaxtomin biosynthetic machinery in the potato common scab pathogen Streptomyces scabies

“…In contrast, the TxtH homologue from the thaxtomin biosynthetic gene cluster of another scab pathogen, S. turgidiscabies, shares only 80% amino acid identity with the S. scabies TxtH. This is consistent with a previous phylogenetic analysis that suggested that the thaxtomin biosynthetic gene clusters from S. scabies and S. acidiscabies are more closely related to each other than to the S. turgidiscabies gene cluster (Huguet‐Tapia et al ., ). As expected, the TxtH homologues from the pathogenic Streptomyces spp.…”

Biological control of potato common scab by Bacillus amyloliquefaciens Ba01

“…Because of the limited understanding of the genetic diversity of S . scabies and the genetic differences in various potato cultivars, developing effective control strategies for potato common scab is challenging [ 6 – 10 ]. Traditional control methods such as soil amendment/chemistry to lower soil pH, soil fumigation with chloropicrin, pre-sowing treatment of seed tubers with fluazinam or flusulfamide, and crop rotation are usually not efficacious and may harm the environment [ 6 , 11 , 12 ].…”

Recent advances in understanding Streptomyces

“…Although scab research has focused on the pathogenicity islands, comparative genomics has revealed 64 other genes that are common to four distinct scab agents but absent from non-pathogens, as well as an exceptionally high proportion of enzymes such as pectinases and cutinases that would aid or take advantage of pathogenicity 35, 40 .…”

“…This accessory genome totalled 32,574 genes, so the Streptomyces pan-genome comprises at least 34,592 genes. The accessory genes are mostly clustered at the chromosome ends, which are well known to be unstable and subject to replacement by recombination with incoming linear plasmids or conjugally transferred segments of chromosomes from other streptomycetes, but recent analyses have revealed an unexpectedly high level of historical recombination within representative core genes too, resulting in phylogenetic incongruence among these genes 40, 43, 44 . The recombination levels detected are high enough to raise the question of whether the evolutionary radiation of the genus has taken place over a significantly shorter time than has been widely accepted 44 .…”